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Nutrition of Marsupial Herbivores Proceedings of the Num'tion Society (1989). 48.69-79 69 Nutrition of marsupial herbivores By 1. D. HUME,School of Biological Sciences, University of Sydney, New South Wales 2006, Australia Mammalian herbivores can be divided into two groups on the basis of the principal site of microbial fermentation. Fore-gut fermenters have an expanded and differentiated fore-stomach. Eutherian fore-gut fermenters include sloths, colobid monkeys, hippos, peccaries, camelids and ruminants. Marsupial fore-gut fermenters include the kanga- roos, wallabies and rat-kangaroos. Hind-gut fermenters have an expanded caecum, proximal colon, or both. They can be divided into caecum fermenters and colon fermenters (Hume & Warner, 1980). In colon fermenters the principal site of microbial fermentation is the proximal colon. A caecum may or may not be present. When it is present, as in the horse, it seems to function largely as a simple extension of the proximal colon. In the only marsupial colon fermenters, the wombats, the caecum is represented by a small vermiform appendix. In caecum fermenters microbial fermentation is more-or-less confined to an enlarged caecum. Eutherian caecum fermenters include rodents (e.g., beaver, porcupine, guinea- pig) and lagomorphs (rabbit, hare, pika). Marsupial caecum fermenters include several arboreal species that specialize on Eucalyptus foliage as food, such as the brushtail possum (Trichosurus vulpecula), ringtail possum (Pseudocheirus peregrinus) and greater glider (Peruuroides volans). The koala (Phascolarctos cinereus), another Eucalyptus specialist, exhibits features of both caecum fermentation and colon fermentation. The present paper reviews research on digestive function and nutrient requirements of marsupial herbivores, based on the general outline of herbivore digestive adaptions outlined previously. Nutrient requirements of marsupial herbivores There is currently much debate over the relative importance of phylogeny and food habits in explaining differences in basal metabolic rates (BMR) between groups of mammals (McNab, 1978; Elgar & Harvey, 1987). Among terrestrial grazer-browsers, macropodid marsupials (i.e., kangaroos and wallabies) and wombats have BMR which are 30% or more below those of eutherians (McNab, 1978). However, among arboreal folivores both eutherians and marsupials have low BMR. The relatively low BMR of macropodid marsupials (Dawson & Hulbert, 1970) is reflected in low maintenance requirements of adult animals for energy (Hume, 1974) and protein (Hume, 1982u), and low turnover rates of water (Hume, 1982b). However, there are exceptions, most of which can be related to differences in habitat between species. As can be seen from Table 1, species which have low maintenance nitrogen requirements are from arid or semi-arid habitats, while those with relatively high requirements are restricted in their distribution to more mesic environments. Requirements for trace minerals such as copper, molybdenum, cobalt and selenium have also been found to be low, at least in the quokka (Setonir brachyurus,) a small wallaby which thrives on Rottnest Island off the Western Australian coast. Early attempts to graze sheep on this island met with failure when the animals quickly developed a wasting disease now known to be a dual deficiency of Cu and Co. The limestone-derived sandy soils of Rottnest Island are poor in their status of most minerals. Barker (1960) concluded that the quokka requires only 3.pg Cu/kg, half the requirement Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 30 Sep 2021 at 16:38:34, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1079/PNS19890011 70 I. D. HUME 1989 Table 1. Maintenance nitrogen requirements of macropodid marsupials (mg truly digestible Nlkg body mass@75per d) Species Habitat Requirement Reference Macropus robustus erubescens Arid scrubland 160 Brown & Main (1967) (euro) M. robustus robustus Woodland 240 Foley et a/. (1980) (wallaroo) M. giganteus Forest. woodland 270 Foley et a/. (1980) (eastern grey kangaroo) M. eugenii Scrub, heath, 250 Barker (1968) (tammar wallaby) dry forest 230 Hume (1977) M. parma Moist forest 477 Hume (1986) (parma wallaby) Thylogale thetis Moist forest, rainforest 530 Hume (1977) (red-necked pademelon) of merino sheep, to maintain normal blood Cu levels. Barker (1961) also showed that this low dietary requirement for Cu could be markedly elevated by the presence of Mo and inorganic sulphate. Thus, the same three-way Cu-Mo-SO4 interaction shown to occur in the induction of Cu deficiency in ruminants (Dick et al. 1975) apparently also occurs in quokkas. This is not surprising, since both quokkas and sheep are fore-gut fermenters. Mineral requirements of strict Eucalyptus feeders such as the koala and greater glider must also be low, since eucalypt foliage is often found to have levels of phosphorus, sodium, zinc, Se and Cu that are below the levels recommended for domestic sheep and horses (Ullrey et al. 1981). However, exact mineral requirements have been defined for very few marsupials. Of the vitamins, only vitamin E has attracted significant attention. This is because of the finding of Kakulas (1961) that captive quokkas from Rottnest Island developed a paralysis of the hind limbs when maintained on a diet of commercial sheep pellets. The same disorder has also been observed with other species of small wallabies maintained on lucerne (Medicago sativa) hay (Hume, 19824. Histologically, there are marked degenerative changes in the muscles of the hind limbs, lesions typical of a deficiency of vitamin E in the diet. These lesions can be reversed by oral dosing of affected wallabies with 200-600 mg vitamin E daily for several days (Kakulas, 1961), but not with Se. In ruminants, and many other species, Se has been found to be an effective substitute for vitamin E. Wallabies (and rabbits) appear to belong to a small group of animals in which nutritional muscular dystrophy is not prevented by trace amounts of Se. Digestive function in marsupial herbivores Hind-gut fermenters. Colon fermenters, both eutherian and marsupial, are typically large. The only marsupial colon fermenters, wombats, are terrestrial grazers of 2545 kg adult body mass. The digestive tract of the common wombat (Vombatus ursinus) is shown in Fig. 1. The caecum is represented by a small vermiform appendix. The colon is large, about 70% of total digestive tract capacity, and, like that of the eutherian horse, is characterized by longitudinal bands of muscle (taeniae), between which are found non-permanent semi-lunar folds, or haustra. Contractions of the colon wall, which form the haustra, are responsible for both the caudal propulsion of digesta and the selective Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 30 Sep 2021 at 16:38:34, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1079/PNS19890011 Vol. 48 Nutrition of non-ruminant herbivores 71 0 100mm u Fig. 1. Digestive tract of the common wombat (Vornbatus ursinus), a colon fennenter, 2545 kg body mass. Drawn from Hume (19820). retention of large particles. The mean retention time (MRT) (Warner, 1981) of particle markers (62-75 h in V. ursinus) is greater than that of fluid markers (36-50 h) (P. S. Barboza, personal communication). Particle markers are also selectively retained in a eutherian colon fermenter, the horse. This maximizes microbial degradation of large particles. Thus, like the horse, the wombat appears well suited to using grasses, which are often of low nutritive value, as a food source. In contrast to colon fermenters, caecum fermenters are typically small. Marsupial caecum fermenters range from the 750 g ringtail possums and 1.2 kg greater glider to 3 kg brushtail possums. The koala, which exhibits features of both caecum fermenters and colon fermenters, is larger, at 8-13 kg. The digestive tract of the greater glider is shown in Fig. 2, and of the koala in Fig. 3. In common with eutherian caecum fermenters, in the ringtail possum, greater glider and koala there is selective retention, not of large particles but of fluid and fine particles (mainly bacteria). For example, in the ringtail possum the MRT of fluid was found to be 63 h, and of particles 35 h (Chilcott & Hume, 1985). The site of this selective retention of Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 30 Sep 2021 at 16:38:34, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1079/PNS19890011 72 I. D. HUME 1989 Oesophagus Fig. 2. Digestive tract of the greater glider (Petuuroides volum), a caecum fcrmenter. 1.2 kg body mass. Drawn from Hume (1982a). fluid in the ringtail possum and greater glider is the caecum, but in the koala both the caecum and proximal colon are involved (Cork & Warner, 1983). The consequence of selective retention of fluid is to concentrate digestive effort on potentially more-digestible soluble components and fine feed particles, and also perhaps to maintain a higher concentration of bacteria in the caecum. Larger, potentially less-digestible feed particles are voided relatively quickly, helping to reduce gut fill. In the smallest caecum fermenter, the ringtail possum, selective retention of fluid and fine particles in the caecum is combined with caecotrophy, a form of coprophagy (Chilcott, 1984). Coprophagy is the ingestion of faeces. Caecotrophy is the ingestion of soft faeces (caecotrophes) which are derived from caecal contents (Homicke & Bjornhag, 1980). In ringtails, caecotrophes contained four times the concentration of N found in hard faeces (Fig. 4), but only 58% of the concentration of neutral-detergent fibre (NDF)(Chilcott & Hume, 1985). It can be calculated that caecotrophy contributes 58% of digestible energy intake and twice the maintenance N requirement of ringtails fed on an entire diet of Eucafyprus foliage (Chilcott & Hume, 1985).
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